Effects of intracolony variability in behavioral development on plasticity of division of labor in honey bee colonies

There is a genetic component to plasticity in age polyethism in honey bee colonies, such that workers of some genotypes become precocious foragers more readily than do workers of other genotypes, in colonies lacking older bees. Using colonies composed of workers from two identifiable genotype groups, we determined that intracolony differences in the likelihood of becoming a precocious forager are a consequence of differences in rates of behavioral development that are also evident under conditions leading to normal development. An alternative hypothesis, that differences in the likelihood of becoming a precocious forager are due to differences in general sensitivity to altered colony conditions, was not supported. In three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single cohort colonies also foraged at relatively younger ages in colonies in which workers exhibited normal behavioral development. In contrast, in three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single-cohort colonies did not show disproportionately more overaged nursing in colonies in which workers exhibited delayed development. These results indicate that genotypic differences in plasticity in age-related division of labor are based on genotypic differences in rates of behavioral development.     

Shifting foraging strategies in colonies of the social wasp Polybia occidentalis (Hymenoptera, Vespidae)

Social insect colonies can be expected to forage at rates that maximize colony fitness. Foraging at higher rates would increase the rate of worker production, but decrease adult survival. This trade-off has particular significance during the founding stage, when adults lost are not replaced. Prior work has shown that independent-founding wasps rear the first workers rapidly by foraging at high rates. Foraging rates decrease after those individuals pupate, presumably reducing the risk of foundress death. In the swarm-founding wasps, colony-founding units have many workers, making colony death by forager attrition less likely. Do swarm-founding wasps show similar shifts in foraging rates during the founding stage? We measured foraging rates of the swarm-founding wasp, Polybia occidentalis at four stages of colony development. At each stage, foraging rates correlated with the number of larvae present, which, in the founding stages, correlated with the number of cells in the new nest. Thus, foraging rates appear to be demand-driven, with the level of demand in the founding stage set by the size of nest that is constructed. During the founding stage, foraging rates per larva were high initially, suggesting that colonies minimize the development times of larvae early in the founding stage. Later in the stage, foraging rates decreased, which would reduce worker mortality until new workers eclose. This pattern is similar to that shown for independent-founding wasps and likely results from conflicting pressures to maximize colony growth and minimize the risk of colony death by forager attrition.     

Regulation of honey bee division of labor by colony age demography

The age at which worker honey bees begin foraging varies under different colony conditions. Previous studies have shown that juvenile hormone (JH) mediates this behavioral plasticity, and that worker-worker interactions influence both JH titers and age at first foraging. These results also indicated that the age at first foraging is delayed in the presence of foragers, suggesting that colony age demography directly influences temporal division of labor. We tested this hypothesis by determining whether behavioral or physiological development can be accelerated, delayed, or reversed by altering colony age structure. In three out of three trials, earlier onset of foraging was induced in colonies depleted of foragers compared to colonies depleted of an equal number of bees across all age classes. In two out of three trials, delayed onset of foraging was induced in colonies in which foragers were confined compared to colonies with free-flying foragers. Finally, in three out of three trials, both endocrine and exocrine changes associated with reversion from foraging to brood care were induced in colonies composed of all old bees and devoid of brood; JH titers decreased and hypopharyngeal glands regenerated. These results demonstrate that plasticity in age-related division of labor in honey bee colonies is at least partially controlled by social factors. The implications of these results are discussed for the recently developed ‘‘activator-inhibitor” model for honey bee behavioral development. Received: 8 November 1995/Accepted after revision: 10 May 1996     

RAPD markers suggest genotypic effects on forager specialization in a eusocial wasp

Genetic variability within insect societies may provide a mechanism for increasing behavioral diversity among workers, thereby augmenting colony efficiency or flexibility. In order to assess the possibility that division of labor has a genetic component in the eusocial wasp Polybia aequatorialis, I asked whether the genotypes of workers within colonies correlated with behavioral specialization. Workers specialized by foraging for one of the four materials (wood pulp, insect prey, nectar, or water) gathered by their colonies. I collected foragers on 2 days from each of three colonies and identified the material the foragers were carrying when collected. I produced random amplified polymorphic DNA (RAPD) markers from the genomic DNA of these foragers and estimated genotypic similarity of foragers based on sharing of variable RAPD marker bands. Contingency tests on 20 variable loci per colony showed statistically significant (P <0.05) biases in RAPD marker frequencies among forager types in the three colonies. Patterns of association of RAPD marker bands with specializations were constant in two colonies, but changed between collection days in one colony. RAPD marker biases suggest that division of labor among workers includes a genetic component in P. aequatorialis. Colony-level selection on variation in division of labor is a possible factor favoring the evolutionary maintenance of high genotypic variability (low relatedness) in epiponine wasp colonies and in other eusocial insects. Received: 18 July 1995/Accepted after revision: 1 October 1995     

Division of foraging labor in ants can mediate demands for food and safety

Solitary foragers can balance demands for food and safety by varying their relative use of foraging patches and their level of vigilance. Here, we investigate whether colonies of the ant, Formica perpilosa, can balance these demands by dividing labor among workers. We show that foragers collecting nectar in vegetation near their nest are smaller than are those collecting nectar at sites away from the nest. We then use performance tests to show that smaller workers are more likely to succumb to attack from conspecifics but feed on nectar more efficiently than larger workers, suggesting a size-related trade-off between risk susceptibility and harvesting ability. Because foragers that travel away from the nest are probably more likely to encounter ants from neighboring colonies, this trade-off could explain the benefits of dividing foraging labor among workers. In a laboratory experiment, we show that contact with aggressive workers results in an increase in the mean size of recruits to a foraging site: this increase was not the result of more large recruits, but rather because fewer smaller ants traveled to the site. These results suggest that workers particularly susceptible to risk avoid dangerous sites, and suggest that variation in worker size can allow colonies to exploit profitably both hazardous and resource-poor patches.Communicated by L. Sundström     

Differential responses of honeybee (<Emphasis Type="BoldItalic">Apis mellifera</Emphasis>) patrilines to changes in stimuli for the generalist tasks of nursing and foraging

Which task a social insect worker engages in is influenced by the worker’s age, genotype and the colony’s needs. In the honeybee, Apis mellifera, genotype influences both the age a worker switches tasks and its propensity of engaging in specialist tasks, such as water collecting, which only some workers will perform. In this study, we used colonies with natural levels of genetic diversity and manipulated colony age demography to drastically increase the stimuli for the generalist tasks of foraging and nursing, which all workers are thought to engage in at some point in their lives. We examined the representation of worker patrilines engaged in nursing and foraging before and after the perturbation. The representation of patrilines among foragers and nurses differed from that of their overall colony’s population. In the case of foraging, over- and underrepresentation of some patrilines was not simply due to differences in rates of development among patrilines. We show that replacement foragers tend to be drawn from patrilines that were overrepresented among foragers before the perturbation, suggesting that there is a genetic component to the tendency to engage in foraging. In contrast, the representation of patrilines in replacement nurses differed from that in the unperturbed nursing population. Our results show that there is a genetic influence on even the generalist tasks of foraging and nursing, and that the way patrilines in genetically diverse colonies respond to increases in task stimuli depends upon the task. The possible significance of this genetic influence on task allocation is discussed. Electronic supplementary material Supplementary material is available in the online version of this article at doi: and is accessible to authorized users.     

Effects of energy requirements and worker mortality on colony growth and foraging in the honey bee

Summary A model of colony growth and foraging in the honey bee (Apis mellifera L.) is presented. It is assumed that summer workers choose a foraging strategy that maximizes colony population by the end of the season subject to the constraint that enough nectar has been stored to sustain the adult population overwinter. The optimal foraging strategy is derived with respect to the number of flowers visited during one foraging trip. A forager that visits many flowers collects a substantial amount of nectar but the probability that the worker returns alive from the excursion decreases accordingly. Using dynamic modelling, I explore the effects on colony growth of colony population, colony energy requirements and mortality rate while foraging. The model shows that when the expected rate of increase in nectar reserves is low, for instance in small colonies or when mortality rate rises rapidly with foraging intensity, workers collect more nectar during each foraging trip. The increase in foraging activity is realized at the expense of colony growth. The main finding is that depending on colony status the foraging strategy that maximizes worker population implies visits to almost any number of flowers. This is in sharp contrast to predictions from traditional foraging models where foraging intensity is assumed to cluster around values that maximize net rate or efficiency. The model suggests that strategies that cluster around rate and efficiency maximization should be viewed as particular solutions to a more general problem.     

Foraging and spatiotemporal territories in the honey ant Myrmecocystus mimicus wheeler (Hymenoptera: Formicidae)

Summary The honey ant Myrmecocystus mimicus is a scavenger, forages extensively on termites, collects floral nectar, and tends homoptera. Individual foragers of M. mimicus usually disperse in all directions when leaving the nest, but there are also groups of foragers that tend to swarm out of the nest primarily in one direction. Such massive departues are usually at irregular intervals, which may last several hours. The results of field and laboratory experiments suggest that these swarms of foragers are organized by a group recruitment process, during which recruiting scout ants lay chemical orientation trails with hindgut contents and simultaneously stimulate nestmates with a motor display and secretions from the poison gland. Usually these columns travel considerable distances (4–48 m) away from the nest, frequently interfering with the foraging activity of conspecific neighboring colonies.To prevent a neighboring colony from access to temporal food sources or to defend spatiotemporal borders, opposing colonies engage in elaborate display tournaments. Although hundreds of ants are often involved during these tournaments almost no physical fights occur. Instead, individual ants confront each other in highly sterotyped aggressive displays, during which they walk on stilt legs while raising the gaster and head. Some of the ants even seem to inflate their gasters so that the tergites are raised and the whole gaster appears to be larger. In addition, ants involved in tournament activities are on average larger than foragers.The dynamics of the tournament interactions were observed in several colonies over several weeks-mapping each day the locations of the tournaments, the major directions of worker routes away from the nest, and recording the general foraging activities of the colonies. The results indicate that a kind of dominance order can occur among neighboring colonies. On the other hand, often no aggressive interactions among neighboring colonies can be observed, even though the colonies are actively foraging. In those cases the masses of foragers of each colony depart in one major direction that does not bring them into conflict with the masses of foragers of a neighboring colony. This stability, however, can be disturbed by offering a new rich food source to be exploited by two neighboring colonies. This invariably leads to tournament interactions.When a colony is considerably stronger than the other, i.e., with a much larger worker force, the tournaments end quickly and the weaker colony is raided. The foreign workers invade the nest, the queen of the resident colony is killed or dirven off, while the larvae, pupae, callow workers, and honey pot workers are carried or dragged to the nest of the raiders. From these and other observations we conclude that young M. mimicus queens are unlikely to succeed in founding a colony within approximately 3 m of a mature M. mimicus colony because they are discovered and killed, or driven off by workers of the resident colony. Within approximately 3–15 m queens are more likely to start colonies, but these incipient groups run a high risk of being raided and exterminated by the mature colony.Although populations of M. mimicus and M. depilis tend to replace each other, there are areas where both species overlap marginally. Foraging areas and foraging habitats of both species also overlap broadly, but we never observed tournament interactions between M. mimicus and M. depilis.The adaptive significance of the spatiotemporal territories in M. mimicus is discussed.     

Inter-colonial selection for the maintenance of cooperative breeding in the ant Pristomyrmex pungens: a laboratory experiment

The queenless ant Pristomyrmex pungens has an unusual social structure, in which all workers reproduce parthenogenetically and help others. Laboratory experiments manipulating the proportion of post-reproductive foragers in the colony at various rates suggested that colonies with 5–10% forager ratios had the maximum efficiency per-worker. This result suggests that the cooperative colonies may be maintained by colony-level natural selection. Non-cooperative mutants that oviposit but do not forage should increase in relative frequency in the colony in the short term. However, decreased colony productivity and the resulting competition among colonies might eliminate colonies dominated by such mutants in the long term. P. pungens has a viscous population without migration between colonies, which may facilitate this process.     

Does a polyandrous honeybee queen improve through patriline diversity the activity of her colony’s scouting foragers?

Recent studies indicate that the foraging success of a honeybee colony is enhanced when it has numerous genetically diverse patrilines because of queen polyandry. We determined whether foraging is improved in part because patriline diversity generates more responsive populations of scouting foragers. Scouts search for new food sources and advertise them with waggle dances to inform other foragers about unexploited discoveries. We moved multiple-patriline and single-patriline colonies to unfamiliar locations so that colonies relied heavily on successful scouts to initiate recruitment and then compared the development of foraging effort between the two types of colonies. More waggle dance signals were produced during the incipient stages of foraging in multiple-patriline colonies compared to single-patriline colonies because scouts reported food discoveries with longer dances. Scouts also returned to multiple-patriline colonies at rates that were two thirds higher than those of single-patriline colonies, although return rates for general forager populations were not significantly different between colony types. The distance of reported food sources from hives increased with time for all colonies, but by the end of their first day in an unfamiliar environment, maximal foraging reach was greater if colonies had multiple patrilines. Most scouts in multiple-patriline colonies came from a minority of scout-rich patrilines that were generally not those from which general forager populations were derived; the presence of such scout-rich patrilines was correlated with the extent of recruitment signaling in colonies. We show how a honeybee colony’s scouting effort is (and is not) enhanced when extremely polyandrous queens produce genetically diverse colonies.     

High social density increases foraging and scouting rates and induces polydomy in Temnothorax ants

Many organisms live in crowded groups where social density affects behavior and fitness. Social insects inhabit nests that contain many individuals where physical interactions facilitate information flow and organize collective behaviors such as foraging, colony defense, and nest emigration. Changes in nest space and intranidal crowding can alter social interactions and affect worker behavior. Here, I examined the effects of social density on foraging, scouting, and polydomy behavior in ant colonies—using the species Temnothorax rugatulus. First, I analyzed field colonies and determined that nest area scaled isometrically with colony mass—this indicates that nest area changes proportionally with colony size and suggests that ants actively control intranidal density. Second, laboratory experiments showed that colonies maintained under crowded conditions had greater foraging and scouting activities compared to the same colonies maintained at a lower density. Moreover, crowded colonies were significantly more likely to become polydomous. Polydomous colonies divided evenly based on mass between two nests but distributed fewer, heavier workers and brood to the new nests. Polydomous colonies also showed different foraging and scouting rates compared to the same colonies under monodomous conditions. Combined, the results indicate that social density is an important colony phenotype that affects individual and collective behavior in ants. I discuss the function of social density in affecting communication and the organization of labor in social insects and hypothesize that the collective management of social density is a group level adaptation in social insects.     

Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera)

Foraging and the mechanisms that regulate the quantity of food collected are important evolutionary and ecological attributes for all organisms. The decision to collect pollen by honey bee foragers depends on the number of larvae (brood), amount of stored pollen in the colony, as well as forager genotype and available resources in the environment. Here we describe how brood pheromone (whole hexane extracts of larvae) influenced honey bee pollen foraging and test the predictions of two foraging-regulation hypotheses: the indirect or brood-food mechanism and the direct mechanism of pollen-foraging regulation. Hexane extracts of larvae containing brood pheromone stimulated pollen foraging. Colonies were provided with extracts of 1000 larvae (brood pheromone), 1000 larvae (brood), or no brood or pheromone. Colonies with brood pheromone and brood had similar numbers of pollen foragers, while those colonies without brood or pheromone had significantly fewer pollen foragers. The number of pollen foragers increased more than 2.5-fold when colonies were provided with extracts of 2000 larvae as a supplement to the 1000 larvae they already had. Within 1 h of presenting colonies with brood pheromone, pollen foragers responded to the stimulus. The results from this study demonstrate some important aspects of pollen foraging in honey bee colonies: (1) pollen foragers appear to be directly affected by brood pheromone, (2) pollen foraging can be stimulated with brood pheromone in colonies provided with pollen but no larvae, and (3) pollen forager numbers increase with brood pheromone as a supplement to brood without increasing the number of larvae in the colony. These results support the direct-stimulus hypothesis for pollen foraging and do not support the indirect-inhibitor, brood-food hypothesis for pollen-foraging regulation. Received: 5 March 1998 / Accepted after revision: 29 August 1998     

The effect of colony size and starvation on food flow in the fire ant,Solenopsis invicta (Hymenoptera: Formicidae)

Summary Food-sharing experiments were performed with laboratory colonies of Solenopsis invicta containing 1000, 10,000, or 20,000 workers and starved for 0, 3, 7, or 14 days. The effect of these variables was measured on the uptake of radioactive sugar water (1 M) by 1% of the colony's workers and on the trophallactic flow of food from these foragers to the remainder of the colony.Patterns of food distribution in small colonies differed significantly from those in larger nests. In 1000-ant nests, small workers more frequently received food than large workers, but in bigger colonies the opposite occurred.Fire ants were adept at distributing sugar water, with food from a few workers rapidly reaching the majority of the colony as foragers donate their crop contents to groups of recipients and these recipients may themselves act as donors.Foragers respond to colony starvation by individually taking up more food and sharing this fluid with a greater proportion of nestmates. Even foragers from satiated colonies can retrieve at least small amounts of liquid.The forager's state of hunger plays an important role in regulating food distribution. In sugar-satiated nests, previously starved foragers are highly successful at passing on labelled sugar whereas prviously fed foragers are not.     

What makes a honeybee scout?

A honeybee colony needs to divide its workforce so that each of the many tasks it performs has an appropriate number of workers assigned to it. This task allocation system needs to be flexible enough to allow the colony to quickly adapt to an ever-changing environment. In this study, we examined possible mechanisms by which a honeybee colony regulates the division of labor between scouts (foragers that search for new food sources without having been guided to them) and recruits (foragers that were guided via recruitment dances toward food sources). Specifically, we examined the roles that the availability of recruitment dances and worker genotype has in the colony-level regulation of the number of workers engaged in scouting. Our approach was threefold. We first developed a mathematical model to demonstrate that the decision to become a scout or a recruit could be regulated by whether a potential forager can find a recruitment dance within a certain time period. We then tested this model by investigating the effect of dance availability on the regulation of scouts in the field. Lastly, we investigated if the probability of being a scout has a genetic basis. Our field data supported the hypothesis that scouts are those foragers that have failed to locate a recruitment dance as predicted by our model, but we found no effect of genotype on the propensity of foragers to become scouts.     

Division of labor during honey bee colony defense

Summary Some worker honey bees respond to major disturbances of the colony by flying around the assailant and possibly stinging; they are a subset of the bees involved in colony defense. These defenders have an open-ended age distribution similar to that of foragers, but defensive behavior is initiated at a younger age than foraging is. Behavioral and genetic evidence shows that defenders and foragers are distinct groups of older workers. Behaviorally, defenders have less worn wings than foragers, suggesting less flight activity. Genetically, defenders differ in allozyme frequencies, demonstrating different subfamily composition from foragers in the same colony. They also differ in allozyme frequencies from guards in the same colony, providing further evidence for division of labor associated with colony defense. We use this information to develop a model for honey bee colony defense involving at least two distinct groups of workers and we propose that the non-guard defenders be called soldiers, due to their important role in colony defense.Offprint requests to: M.D. Breed     

Aging and demographic plasticity in response to experimental age structures in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L)

Honeybee colonies are highly integrated functional units characterized by a pronounced division of labor. Division of labor among workers is mainly age-based, with younger individuals focusing on in-hive tasks and older workers performing the more hazardous foraging activities. Thus, experimental disruption of the age composition of the worker hive population is expected to have profound consequences for colony function. Adaptive demography theory predicts that the natural hive age composition represents a colony-level adaptation and thus results in optimal hive performance. Alternatively, the hive age composition may be an epiphenomenon, resulting from individual life history optimization. We addressed these predictions by comparing individual worker longevity and brood production in hives that were composed of a single-age cohort, two distinct age cohorts, and hives that had a continuous, natural age distribution. Four experimental replicates showed that colonies with a natural age composition did not consistently have a higher life expectancy and/or brood production than the single-cohort or double-cohort hives. Instead, a complex interplay of age structure, environmental conditions, colony size, brood production, and individual mortality emerged. A general tradeoff between worker life expectancy and colony productivity was apparent, and the transition from in-hive tasks to foraging was the most significant predictor of worker lifespan irrespective of the colony age structure. We conclude that the natural age structure of honeybee hives is not a colony-level adaptation. Furthermore, our results show that honeybees exhibit pronounced demographic plasticity in addition to behavioral plasticity to react to demographic disturbances of their societies.     

Limited flexibility in the temporal caste system of the honey bee

Caste theory predicts that social insect colonies are organized into stable groups of workers specialized on particular task sets. Alternative concepts of organization of work suggest that colonies are composed of extremely flexible workers able to perform any task as demand necessitates. I explored the flexibility of workers in temporal castes of the honey bee Apis mellifera by determining the ability of colonies to reorganize labor after a major demographic disturbance. I evaluated the flexibility of temporal castes by comparing the foraging rates of colonies having just lost their foragers with colonies having also lost their foragers but having been given a week to reorganize. The population sizes and contents of the colonies in each group were equalized and foraging rates were recorded for one week. Colonies given a weeks initial recovery time after the loss of their foragers were found to forage at significantly higher rates than those colonies given no initial recovery time. This result was consistent for nectar and pollen foraging. These results suggest that honeybee workers lack sufficient flexibility to reorganize labor without compromising foraging. This finding is consistent with the caste concept model of organization of work in insect societies.     

Social influences on body size and developmental time in the bumblebee Bombus terrestris

In many social insects, including bumblebees, the division of labor between workers relates to body size, but little is known about the factors influencing larval development and final size. We confirmed and extend the evidence that in the bumblebee Bombus terrestris the adult bee body size is positively correlated with colony age. We next performed cross-fostering experiments in which eggs were switched between incipient (before worker emergence) and later stage colonies with workers. The introduced eggs developed into adults similar in size to their unrelated nestmates and not to their same-age full sisters developing in their mother colony. Detailed observations revealed that brood tending by the queen decreases, but does not cease, in young colonies with workers. We next showed that both worker number and the queen presence influenced the final size of the developing brood, but only the queen influence was mediated by shortening developmental time. In colonies separated by a queen excluder, brood developmental time was shorter in the queenright compartment. These findings suggest that differences in body size are regulated by the brood interactions with the queen and workers, and not by factors inside the eggs that could vary along with colony development. Finally, we developed a model showing that the typical increase in worker number and the decrease in brood contact with the queen can account for the typical increase in body size. Similar self-organized social regulation of brood development may contribute to the optimization of growth and reproduction in additional social insects.     

The use of simulation modeling to evaluate the mechanisms responsible for the nutritional benefits of food-for-protection mutualisms

In some mutualisms, a plant or insect provides a food resource in exchange for protection from herbivores, competitors or predators. This food resource can benefit the consumer, but the relative importance of different mechanisms responsible for this benefit is unclear. We used a colony-level simulation model to test the relative importance of increased larval production, increased worker foraging and increased worker survival for colony growth of fire ants, Solenopsis invicta, that consume plant-based foods. Increased food for larvae had the largest effect on colony growth of S. invicta followed by decreased worker mortality. Increased foraging rate had a small effect in the simulation model but data from a small laboratory experiment and another published study suggest that plant-based foods have little or no effect on foraging rates of S. invicta. Colony growth steadily increased the longer plant-based food was available and colonies were most responsive to plant-based food in the early summer (i.e., June). Our results demonstrate that population level simulation modeling can be a useful tool for examining the ecology of mutualistic interactions and the mechanisms through which species interact.     

Regulation of pollen foraging in honeybee colonies: effects of young brood, stored pollen, and empty space

Pollen storage in a colony of Apis mellifera is actively regulated by increasing and decreasing pollen foraging according to the “colony's needs.” It has been shown that nectar foragers indirectly gather information about the nectar supply of the colony from nestmates without estimating the amount of honey actually stored in the combs. Very little is known about how the actual colony need is perceived with respect to pollen foraging. Two factors influence the need for pollen: the quantity of pollen stored in cells and the amount of brood. To elucidate the mechanisms of perception, we changed the environment within normal-sized colonies by adding pollen or young brood and measured the pollen-foraging activity, while foragers had either direct access to them or not. Our results show that the amount of stored pollen, young brood, and empty space directly provide important stimuli that affect foraging behavior. Different mechanisms for forager perception of the change in the environment are discussed. Received: 13 June 1998 / Accepted after revision: 25 October 1998